A peer-reviewed open-access journal NeoBiota 70: 123—150 (2021) doi: 10.3897/neobiota.70.68202 &) NeoBiota https:/ / neobi ota. pen soft. net Advancing research on alien species and biological invasions Management of invasive alien species in Spain: A bibliometric review Rafael Mufoz-Mas', Martina Carrete?, Pilar Castro-Diez?, Miguel Delibes-Mateos*, Josep A. Jaques’, Marta Lopez-Darias®, Manuel Nogales®, Joan Pino’®, Anna Traveset’, Xavier Turon'®, Montserrat Vila''!?, Emili Garcia-Berthou! | GRECO, Institute of Aquatic Ecology, University of Girona, 17003 Girona, Spain 2 Departamento de Sistemas Fisicos, Quimicos y Naturales, Universidad Pablo de Olavide, Ctra. de Utrera, km. 1 41013, Seville, Spain 3 Biological Invasions Research Group (Biolnv), Departamento de Ciencias de la Vida, Universidad de Alcala, Pza. San Diego, s/n, 28801, Alcala de Henares, Madrid, Spain 4 Instituto de Estudios Sociales Avan- zados (IESA-CSIC), Plaza Campo Santo de los Martires, 7, 14004 Cordoba, Spain § Departament de Cién- cies Agraries i del Medi Natural, Universitat Jaume I, Av. Vicent Sos Baynat, s/n, 12071 Castellé de la Plana, Spain 6 Island Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiologia (IPNA- CSIC), Avda. Astrofisico Francisco Sanchez, 3, 38206 - San Cristébal de La Laguna Santa Cruz de Tenerife - Islas Canarias, Spain 7 CREAE E08193 Bellaterra (Cerdanyola del Valles), Catalonia, Spain 8 Universitat Autonoma de Barcelona, E08193 Bellaterra (Cerdanyola del Valles), Catalonia, Spain 9 Instituto Mediterrd- neo de Estudios Avanzados (IMEDEA, CSIC-UIB), C/ Miquel Marques, 21 - 07190 Esporles , Mallorca, Illes Balears, Spain \0 Departamento de Ecologia Marina, Centro de Estudios Avanzados de Blanes (CEAB-CSIC), Accés a la Cala St. Francesc, 14, 17300 Blanes, Spain \\ Estacién Biolégica de Donana (EBD-CSIC), Avda. Américo Vespucio 26 ,41092 Sevilla, Spain \2 Department of Plant Biology and Ecology, University of Sevilla, 41012 Sevilla, Spain Corresponding author: Rafael Mufioz-Mas (rafa.m.mas@gmail.com) Academiceditor: Moritz von der Lippe | Received 3 May 2021 | Accepted 22 October 2021 | Published 14 December2021 Citation: Mufoz-Mas R, Carrete M, Castro-Diez P, Delibes-Mateos M, Jaques JA, Lépez-Darias M, Nogales M, Pino J, Traveset A, Turon X, Vila M, Garcia-Berthou E (2021) Management of invasive alien species in Spain: a bibliomet- ric review. NeoBiota 70: 123-150. https://doi.org/10.3897/neobiota.70.68202 Abstract Scientific and grey literature on invasive alien species (IAS) is conditioned by social, economic and politi- cal priorities, editorial preferences and species and ecosystem characteristics. This leads to knowledge gaps and mismatches between scientific research interests and management needs. We reviewed the literature on IAS management in Spain found in Scopus, Web of Science, Google Scholar and Dialnet to identify key deficiencies and priority research areas. The collected literature was classified, employing features Copyright Rafael Mufioz-Mas et al.. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 124 Rafael Mufioz-Mas et al. / NeoBiota 70: 123—150 (2021) describing formal aspects and content. We used bibliometric and keyword co-occurrence network analy- ses to assess the relationship between features and reveal the existence of additional topics. Most of the compiled documents (n = 388) were focused on terrestrial ecosystems and inland waters, whereas marine and urban ecosystems were under-represented. The literature was largely generic and not species-specific, focusing on raising awareness and proposing changes on current regulation as prominent approaches to prevent further introductions. The compiled authors exhibited many clear publishing preferences (e.g. language or document type), but less regarding target taxa. In addition, there was a strong association between species and the different features considered, especially between the methodological approach (e.g. review, field experiment) and the primary emphasis of study (i.e. basic/theoretical, applied or inter- disciplinary). This indicates that research on IAS has had a strong species-specific focus. References about terrestrial species focused mainly on vascular plants, whereas references about inland waters were mostly on fishes and the giant reed (Arundo donax), which has been managed with partial success. Animal cull- ing and plant removal were the most frequent eradication and small-scale control treatments, whereas the documents addressing wider spatial scales were largely theoretical. Consequently, the success of described treatments was largely uncertain. Spanish invasion science research has been occasionally innovative, in- corporating novel technologies (e.g. species distribution modelling) and engaging society with citizen- science approaches. However, the ratio between basic/theoretical and applied studies indicates that more applied research/management is needed, especially in inland waters and marine ecosystems. We call for increasing effort in the effective dissemination of experience in IAS management to enhance current prac- tical knowledge, including that of schemes undertaken by public agencies. Keywords Biological invasions, eradication, control, Iberian Peninsula, Mediterranean, Spanish archipelagos, key- word co-occurrence analysis, prevention Introduction Biological invasions are human-assisted global phenomena with ravaging effects, not only on biodiversity and ecosystem services, but also on human well-being (McGeoch et al. 2010; Vila and Hulme 2017). Although transport and introduction of alien species into novel ecosystems is inherent to humankind’s expansion (Crees and Turvey 2015), the number of new introductions has increased exponentially since the mid-twentieth century (Seebens et al. 2018, 2019). Invasive alien species (IAS) can reshape ecosystem processes, decrease native species richness and abundance (e.g. McGeoch et al. 2010 and references therein) and cause impact on the economy and human health (Zenni et al. 2021). Thus, preventative, eradication and control actions are required to impede their entry and establishment or minimise their long-term impacts (Robertson et al. 2020). The incidence of biological invasions and their related costs have led to substantial management efforts worldwide to prevent new introductions and control those already established, by means of eradication or containment (Garcia-de-Lomas and Vila 2015; Diagne et al. 2021). However, to offer efficient responses is challenging and, regretta- bly, the specific literature on IAS management is often neglected during the decision- making process (Walsh et al. 2015). In Spain, managers, consultants and assessors face obstacles to find and access suitable references, as a large proportion of papers are written in English, are too scientifically orientated or narrowly focused to be directly Review of invasive alien species management literature from Spain 125 applied or are not open-access (Andreu and Vila 2007; Mungi et al. 2019; Copp et al. 2021). In addition, many applied studies are scattered amongst the grey literature (often in many different languages), tending to be largely inaccessible to international readers, which further limits the transfer of knowledge on both local and international levels (Haddaway and Bayliss 2015, Jeschke et al. 2019). In addition to accessibility barriers, the content of scientific literature is also taxo- nomically and geographically biased (Hulme et al. 2013). This is accentuated by the fact that reviews and positive rather than negative results are more likely to be pub- lished (Fanelli 2012). Thus, several characteristics inherent to IAS and recipient ecosys- tems utterly favour the availability of literature on specific taxa, regions or ecosystems that are easier to study and/or manage (Thomsen et al. 2014; Nghiem et al. 2016; Shackleton et al. 2019). Moreover, trends in invasion science are also affected by so- cial and political priorities, which are, in turn, influenced by communication media and the outcomes of previous research (Glaser and Laudel 2016; Geraldi et al. 2019; Shackleton et al. 2019). This can lead to changes in the importance of research topics over time, for instance through fostering a given species over others or by abandoning certain research areas. Bibliometric and keyword co-occurrence network analyses are useful to reveal the main knowledge components of any discipline, such as areas with deep insights, out- standing gaps and peripheral research areas (Aria and Cuccurullo 2017, Radhakrishnan et al. 2017). Despite some recent contributions (Enders et al. 2019, 2020), such analy- ses are scarce in previous reviews of IAS literature, particularly related to management. Consequently, we chose to use them to identify the main patterns in the scientific lit- erature shown by IAS management in Spain. Our specific aims were to: (i) characterise the species, topics and approaches from a management viewpoint, (ii) detect relation- ships between them and (iii) identify research areas deserving further attention. We focused on Spain due to its diversity of climates and ecosystems, along with its insular and continental territories, which have favoured the establishment of a large and di- verse number of IAS (Mufioz-Mas and Garcifa-Berthou 2020). Mainland Spain is part of the Mediterranean biodiversity hotspot (Williams et al. 2011) and encompasses an enormous range of ecosystem types, from arid coastal regions to mountain ranges and woodlands. Spain includes two markedly-different populated archipelagos: the Medi- terranean Balearic Islands and the Macaronesian Canary Islands off the north-western African coast (Andreu et al. 2009; Benito-Calvo et al. 2009). Islands are in themselves biodiversity hotspots, but they have especially suffered from the establishment of IAS, which have caused numerous extinctions (Lenzner et al. 2020). In addition, Spain has two autonomous cities located on the Mediterranean coast of the African continent, which may require different [AS management approaches. Former reviews on invasion management in the country were sectorial and focused on stakeholder perceptions and management of alien plants (Andreu et al. 2009) or were based on the most common deficiencies in [AS management (Dana et al. 2019). Thus, reviewing past and present experience may help to improve current IAS management actions and identify future research lines in Spain and similar territories. Our results may help funding agencies to target as yet unidentified research needs. 126 Rafael Mufioz-Mas et al. / NeoBiota 70: 123—150 (2021) Methods Literature review We performed our literature search using Scopus, Web of Science (WoS) and Google Scholar. The first two mainly focus on English language literature, largely scientific papers, whereas the references compiled within Google Scholar are more heterogeneous and less structured (Haddaway et al. 2015). Monolingual searches have been shown to limit and bias results in global literature reviews (Angulo et al. 2021; Nufez and Amano 2021). To avoid such potential bias, in addition to Google Scholar, we also consulted Dialnet. This is a multidisciplinary reference database launched in 2001 that focuses on scientific literature published in Spanish, including books, theses and other documents. We used the following search terms in Scopus and WoS (both accessed 28 April 2020): (Spain OR Iberian Peninsula OR Canary Islands OR Balearic Islands OR Ceu- ta OR Melilla) AND (alien species OR exotic species OR non-native species OR in- vasive species OR introduced species OR species introduction OR translocated species OR species translocation OR species spread OR naturalised species OR casual species OR species of concern OR noxious species OR pernicious species OR harmful spe- cies) (Rytwinski et al. 2020). We also used the equivalent Spanish terms for searches in Google Scholar and Dialnet, the latter accessed 30 May 2020. The results were down- loaded from Scopus, WoS and Dialnet and duplicates removed (Rytwinski et al. 2020) (Table 1). Following Rytwinski et al. (2020), we modified this general workflow for searches in Google Scholar to deal with the inferior specificity of the searching engine. Between 29 April and 30 May 2020, we retrieved up to 1,000 documents, including duplicates, starting the search using the Spanish keywords describing the toponymy (e.g. Espafia or peninsula Ibérica) and terms used to name IAS (e.g. especie exotica or especie invasora) with one of the following terms: gestién (management), erradicacién (eradication) or control. Starting with gestién, we selected documents up to the point when they were clearly irrelevant or duplicated. We then repeated the query using the following keyword (first erradicacién and finally control) and repeated the entire pro- cess using the English keywords. Once 1,000 documents were compiled, the full text was checked to discard irrelevant documents and, only then, we added the document to the references obtained from Scopus and WoS (Table 1). Only documents focusing on direct IAS management (i.e. eradication and con- trol) or with explicit management implications in Spain were included (e.g. risk assessment and prevention of future invasions, regulations or education). Studies exclusively focusing on the biology or the ecology of IAS, with no management implications or with no examples, were discarded. We only counted introduced and established species or species able to spread in the wild (e.g. Blackburn et al. 2011), excluding those in captivity or cultivated. We also considered microorganisms and parasites (potentially) affecting other species in the wild (e.g. the crayfish plague Aphanomyces astaci or the amphibian chytrid fungus Batrachochytrium dendroba- tidis), but excluding agricultural pests or pathogens of captive animals or humans. Review of invasive alien species management literature from Spain AQF In general, no agriculture-related studies were retained, nor weeds interfering with crops or plantations. However, studies on the red weevil, Rhynchophorus ferrugineus, were not excluded, although they focused on the date palm Phoenix dactylifera, be- cause this weevil also affects the endemic Canary Islands date palm Phoenix canar- iensis. We compiled a total of 388 documents (Table 1). Literature characterisation and keyword compilation We selected relevant features of the retrieved documents for our analysis, follow- ing previous bibliographic studies on IAS management (mostly Bayliss et al. 2013; Matzek et al. 2014) (Table 2). The selected features described formal aspects (e.g. Table |. Total number of references retrieved before scrutiny (e.g. including duplicates) and final number of references retained for the database. Web of Science and Scopus were managed simultaneously because they show a great overlap of hosted references. Bibliographic database Number of references retrieved Number of references retained Scopus 1569 14 Web of Science 1152 Dialnet 7p) 62 Google Scholar 1000 Ly? Table 2. Features and categories used to characterise the compiled literature (based on Andreu and Vila 2007; Bayliss et al. 2013; Matzek et al. 2014). Specific definitions for each category of the selected features are provided in Supplementary Material (Table S1). Feature Categories Authors e Document type _ Scientific article, book, book chapter, conference proceedings, report or thesis Ecological organi- Population/autoecology, community/assemblage, ecosystem or generic/not applicable sation level Ecosystem type Terrestrial, inland waters, marine or urban Insular territory Yes or no Language English or Spanish Main topic Management (eradication and control), prediction, prevention, prioritisation (including risk manage- ment), regulation/decision-making, risk assessment, social, biology/ecology, climate change and other syhergisms, conservation, definitions, economics, education and awareness-raising, impacts, informa- tion sharing, communication and collaboration, introduction/spread or survey/monitoring Management topic Prevention, eradication, control or generic/not applicable Methodological — Review/meta-analysis, observational field study, field experiment, greenhouse/laboratory experiment, approach opinion paper or theory Primary emphasis Basic (without direct manipulation of the target taxa), applied (with direct manipulation of the target taxa) or interdisciplinary (encompassing social and policy issues) Protected area Yes or no Spatial scale Local, regional, national, supranational/global or other/undefined (e.g. greenhouse/lab experiment) Species Target species, taxon or generic/multiple taxa Success Yes, partial, no, unknown or not applicable Treatment Regulation, awareness raising, culling, biocontrol agent, poisoning, hydrology manipulation, hydrogeo- morphological restoration, survey and monitoring, mechanical removal, manual removal, herbicide, genetic selection, exclosure, not applicable, DNA metabarcoding, re-afforestation, heating, baiting, containment, mulching, prevention, restocking, incineration, insecticide or sterilisation Year 2 128 Rafael Mufioz-Mas et al. / NeoBiota 70: 123—150 (2021) document type or text language) and content (e.g. methodological approach, main topic, spatial scale). To better characterise documents with multiple topics and sec- tions, the categories within the different features were non-exclusive. That is, a docu- ment could focus on the biology/ecology, introduction/spread and survey/monitor- ing of IAS or on prevention, eradication and control. However, during subsequent analyses, we downweighed each reference in the frequency-related calculations to sum up to one and ensure the equal contribution of all documents (Mufioz-Mas and Garcia-Berthou 2020). We downloaded the keywords from documents retrieved from Scopus and WoS and manually scrutinised those documents compiled from Google Scholar and Dialnet to compile the available keywords. Then, we inspected the keywords to detect mistakes and misspellings and translated those words into Spanish using Google Translator, adjusting English keywords to well-established terms when necessary (e.g. cafia comtin/common reed to giant reed). The references and features can be found in Supplementary Material. Data analyses We used the cumulative sum of number of documents per year to compare the pub- lishing trends in management of invasive alien species in Spain with more general science publishing trends (in Spain and worldwide). The total number of documents published worldwide and in Spain were those included in the Journal Citation Re- ports (JCRs). The series were retrieved from: www.scimagojr.com/countryrank.php. Frequency bar plots enabled scrutiny of the prevalence of the different categories of each additional feature, except species and ecosystem types. We investigated these two features simultaneously using the function comparison.cloud of the R (R Core Team 2021) package wordcloud (Fellows 2018), but without graphical scrutiny for language, insular territory or protected area, due to their binary nature. The association amongst features was analysed, except year (Table 2), employing Cramér's V Index (Cramér 1946), implemented in the R package oii (Hale et al. 2017). This Index ranges from 0 (no association) to 1 (perfect association) and is based on a corrected ¥’ statistic. To graphically describe the association patterns, we built a network using the R package igraph (Csardi and Nepusz 2006), employing the values of the Index only when statistically significant (P < 0.05). Cramér's V Index evaluates the association between features, but provides no in- formation about the relationship amongst categories. Therefore, we built two alluvial diagrams to graphically scrutinise the relationship between the categories of the features: methodological approach, ecosystem type, management topic and spatial scale and eco- system type, treatment and success (Table 2). Alluvial diagrams are a kind of Sankey dia- gram that group together observations of the same category and visualise them as flows across the considered set of features (Rosvall and Bergstrom 2010). We used the function SankeyDiagram in the R package flipPlots (Displayr 2019) to build the alluvial diagram. To investigate the existence of additional topics and research areas not described by the features and categories detailed in Table 2, we analysed the literature using a Review of invasive alien species management literature from Spain 129 keyword co-occurrence network (Radhakrishnan et al. 2017). As customary, we first systematically lemmatised/stemmed the resulting keywords in R (i.e. inflected or de- rived words were reduced to their root form) to reduce the variability within the col- lected keywords. For example, by applying this procedure, the word biolog would result from the words biological and biology. For this, we used the function word- Stem of the R package SnowballC (Bouchet-Valat 2020) to allow reproducible results. Compound keywords were split (e.g. invasive species was divided into invasive and species), each word was lemmatised independently (e.g. invas and speci) and the result- ing words were reassembled (e.g. invas speci) to build the co-occurrence network. The co-occurrence matrix cross-product was obtained via the function cocMatrix of the R package bibliometrix (Aria and Cuccurullo 2017) and we built the co-occurrence network with igraph (Csardi and Nepusz 2006). We delineated the relevant research areas or clusters employing the function cluster_edge_betweenness (Newman and Gir- van 2004) in igraph (Csardi and Nepusz 2006). Finally, the most frequent keyword of each cluster was used to simplify the complete network into a smaller network and facilitate its interpretation. To avoid oversimplification of the network, we kept the most frequent keywords (> Q,. or number of occurrences = 4 occurrences), while the less frequent keywords were collapsed to the most frequent keyword in the correspond- ing research area (i.e. the cluster centre). We depicted the resulting network with the most important keywords in each research area (i.e. cluster centres encompassing the most frequent and less frequent keywords into single vertices and additionally those keywords whose frequency of occurrence was = 4) as two-level circular treemaps (Zhao and Lu 2015) using the R package ggraph (Pedersen 2021). Results The number of documents published on IAS management has grown steadily since 1995 (Figure 1A). However, those published in Spain are under-represented compared to the scientific production trends both globally and in Spain, although during the last decade, the scientific production accelerated significantly. Most documents were scien- tific articles (72.4%) (Figure 1B). Review/meta-analysis was the most common meth- odological approach (54.9% out of the 388 documents), followed by field experiment (19.0%) and observational field study (18.9%) (Figure C). The total number of au- thors was 1,280. The most prolific author was Montserrat Vila (13 documents/3.4%), followed by Pilar Castro-Diez, Elfas D Dana and Juan Garcia de Lomas (7 documents each/1.8%), whereas 1,067 authors appeared in one single document (Figure 1D). Most documents were written in English (59.3%) and the remainder in Spanish. Management (i.e. eradication and control) was the most frequent topic (31.8% out of 388 documents), followed by risk assessment (9.6%), survey/monitoring (9.3%), biology/ecology (7.6%), and impacts (7.4%) (Figure 2A). Studies focusing on popula- tions and the autoecology of a single species were the most frequent (45.2%), followed by studies at the community/assemblage level (24.0%) (Figure 2B). The dominant 130 Rafael Mufioz-Mas et al. / NeoBiota 70: 123—150 (2021) > w Cc 1.6e+06 - 6.5e+07 7 337 -— = Spain — IAs nt eps ; . : 2 au maa Scientific articles —— | Review/meta-analysis —<—| 5 ° E 1.2e+06 + 4.9e+07 — 290 Theses [ Field experiment [| 5) fe) 2 Books [| Obs. field study [| © 81e+05 5 3.2e+07 — 194 9 Reports | Greenhousellab exp. ll = 2 4.1e+054 1.6e+07 4 97 Conf. proceedings | Opinion I o > to Book chapters | Theory | Z 0.0+00 ~ 0.0e+00 0 a ee | a i el ) 1995 2005 2015 0 50 150 250 0 50 450 250 Year Number of documents Number of documents D 14 € 12 = 10 3 o 68 x?) o 6 = 2 4 35 2 z 0 SQQ>7°PIWIY SDS SOSSSCWSIOS PPULKMSA47 10 0I1f SOM MO 2OU dt e5[TSOrh bh oM— eo oew SN sees ed ods ESH Pes C SS EO See O GT EE ESB ES SS te Peet gs ONS Seg SI GPO ISTE CS ROS GOSS TNE GF KOTO FOSS IS SRS CSR OG sac BoKEIZES ES FO GSES EOS ET CUES BEE OFA BSE S SAS SRS HOS PN HSORPS ESS VZ Reso E SLOSS Sor-gogasa zZEOD SOn=2 oa L228 Seoeese su sten oF 28 LO3t eg 2HSGGS°WZISS9— CQ WIE DoHeoSse SS0SHSES CRBaIS CL SaHE a 2 = < OPGNBUGE 2a er 6 OFS N TL£t5 SIES oN GS BY g og w Soa 5 8 o -34 Sns osha Oo s 86 B83 > 2 5 Oo 4 a a>@2 sae” o > => —t => G = i= s 36 3-28 fe) 2 ar a Ee s 68 O a 8 & oa a 0) Ss 2 Figure |. Cumulative number of documents on IAS management in Spain and cumulative number of scientific documents included in the Journal Citation Reports (JCRs), with no distinction by research area (A). Global series encompasses all the documents included in the JCRs, whereas the Spain series includes exclusively those produced in Spain (data retrieved from www.scimagojr.com/countryrank.php). Numbers of documents by types are represented in (B), methodological approaches in (C) and number of documents by the most prolific authors in (D). management topic was generic/not applicable (48.0%) — i.e. documents that did not focus on prevention, eradication or control of IAS and did not involve direct ma- nipulation of target [AS — followed by control (22.7%), whereas studies focusing on prevention and eradication were less frequent (17.5% and 11.7%, respectively) (Figure 2C). Studies on a local or national scale were more frequent (28.9% and 24.2%) than those on the intermediate (regional) or largest (supranational/global) scales (20.6% and 18.6%, respectively) (Figure 2D). The most frequent primary emphasis was ba- sic (i.e. without direct manipulation of target taxa) (45.6%), followed by applied or interdisciplinary scopes (i.e. encompassing social and policy issues), both with similar prevalence (28% and 25.5%, respectively) (Figure 2E). The most frequent manage- ment treatments concerned impeding the establishment of further IAS through aware- ness-raising, regulation and survey monitoring (18.0%, 15.3% and 11.8%, respec- tively) (Figure 2F). Animal culling (9.1%) and plant mechanical and manual removal (11.5%) were the most common eradication and control treatments, whereas 8.2% of documents did not report specific treatments of target IAS (i.e. not applicable). The success of the proposed treatments as eradication or control methods was largely uncertain (not applicable/42.8% or unknown/23.4%) or partial (15%), which implies Review of invasive alien species management literature from Spain 131 . Awareness raisin Management = Population/autoecology al Pselaten _ Risk assessment O Survey and monitoring [i Survey/monitoring ] Community/assemblage a Culling Ei Biology/ecology Q] at ang = : : ; Mechanical removal indole nl Generic/Not applicable |] Manual removal [i : Reafforestation [J Introduction/spread 0 Ecosystem [| Herbicide [i Regulation decision-making Al an Sen SSeS Hydrology manipulation [fj Prediction (| ' Exclosure [fj 0 50 100 200 Biocontrol agent ff Social i Poisoning fj ‘ i Number of documents Hydrogeomorph. rest. fj Inf. sharing, comm. & collaboration i : 5 Cc Genetic selection | Education & awareness raising l Insecticide | ; DNA metabarcoding | Economics |] Generic/Not applicable Restocking | Prevention l Baiting | Prioritisation l Control Containment | Incineration | Climate change & synergisms | Ah Heating | Conservation | Eradication Sterilisation | 1e% Prevention | Definitions | Prevention Mulching | 0 100 200 0 50 100 200 0 50 100 200 Number of documents Number of documents Number of documents Local a Not applicable il Basic National [] Unknown | Regional [| Applied Partial [ana Supranational/global lal No [| Other [| Interdisciplinary Yes [| 0 100 200 0 50 100 200 0 50 100 200 Number of documents Number of documents Number of documents Figure 2. Numbers of documents by main topics are represented in (A), ecological organisation levels in (B), management topics in (C), spatial scales in (D), primary emphasis in (E), treatment in (F) and success in (G). sustained management actions to control the target IAS (Figure 2G). About 13% of the studies focused exclusively on insular territories and 17% on protected areas. The compiled studies involved 159 species or higher taxa (e.g. vascular plants). The largest number dealt with terrestrial ecosystems (50.4%), followed by inland waters (36.2%), whereas marine ecosystems and urban environments were the least com- mon (8.3% and 5.0%, respectively) (Figure 3). Terrestrial vascular plants (10.4%) were the most frequent, especially eucalypts (Eucalyptus spp.) (1.6%), prickly pear species (Opuntia spp.) (1.3%), Hottentot figs (Carpobrotus spp.) (1.3%), Monterey pine (Pi- nus radiata) (1.3%) and cordgrasses (Spartina spp.) (1.0%). Amongst terrestrial ani- mals, the most frequent species were the yellow-legged hornet (Vespa velutina) (1.6%), the pinewood nematode Bursaphelenchus xylophilus (1.3%), American mink Neovison vison (1.0%) and generic studies on vertebrates (3.3%), mainly birds (1.3%). In in- land waters, generic studies were also the most common (7.5%), followed by those on fish management (7.0%). The most studied species in inland waters were the giant reed (Arundo donax) (3.1%) and the red swamp crayfish (Procambarus clarki) (1.8%), followed by generic studies on riparian vegetation (1.6%). Most studies on marine 132 Rafael Mufioz-Mas et al. / NeoBiota 70: 123—150 (2021) Cortaderia selloana Myiopsitta monachus Ab getulus Acacia sp Herpestes ichneumon Xylella dines Dryocosmus kuriphilus Felis silvestris catus Aedes albopictus TestudinesSpartina spp. Rhynchophorus ferrugineus Dreissena polymorpha Erwinia amylovora Ailanthus altissi sell spp. Sursaphelenchus xylophilus Cyprinus carpio Ar undo donax Linepithema humile Salve Wis ae mf Tani Mammals Psittacula spp. rocambarus Clarkii G vcahepeaems CONGTIC casei a ys | | Gambusia spp. e N eC a CPinus fadiata., "Meade Eucalyptus spp. ith Eucalyptus spp. Opuntia spp. Macroinvertebrates eC l Carpobrotus spp. pi ica e [ Aves __Neovison vison Fish SPEEA on SS 3] { Vespa velutina Algae a N S G e Nn e rl CG Aedes eta Polychaetes Ayes Psittacula spp. Othe r Ge al e rl C Myiopsitta monachus @ Terrestrial @ Inland waters ™ Marine ™ Urban Figure 3. Word cloud depicting the proportion of documents per ecosystem type and taxon obtained using the function comparison.cloud of the R package wordcloud (Fellows 2018). The species or taxa oc- curring in less than two documents have been grouped within the category Other. Frequencies have been square root-transformed to facilitate reading the species. environments were generic (4.4%) or focused on algae (1.8%) or polychaetes (1.3%). In urban environments, generic (2.1%) and bird studies (0.8%) prevailed, in addition to those on tiger mosquito (Aedes albopictus) (0.5%). The association network displaying Cramér’s V Index between pairs of features in- dicated great specificity regarding authors’ preferences about publishing language and document type and on the management scales and treatment success of the conveyed experiences and approaches (Cramér’s V > 0.91), but inferior regarding the target spe- cies (Cramér’s V = 0.76). Subsequently, the association network highlighted the strong association between species and all other features (Cramér’s V > 0.50), except with document type and protected area (Figure 4). The highest association of this group occurred between species and ecosystem type (Cramét’s V = 0.66) and between species and insular territory (Cramér’s V = 0.65). The connections between species, methodo- logical approach and primary emphasis, as well as those amongst the latter two, were noteworthy. There was no strong association between the remaining features, except between the main topic and primary emphasis and the management topic (Cramér’s V > 0.50). Insular territory and especially document type depicted the lowest association with the remaining features. Review of invasive alien species management literature from Spain 133 LanguageEcosystem Main type topic /? Protected aréa Insular - 1.0 territory Treatment Cramér's V 0.5 Methodological approach ‘ Ecological. 0.0 organisation) Pe. . leve|/ManagementSpecies topic Figure 4. Association network displaying Cramér’s V between features characterising the documents on IAS management in Spain. Connections are only depicted when the ¥’ statistic is significant (P < 0.05). Connection width and colour are based on Cramé1’s V and range from 0 (no association) to 1 (perfect association). The most frequent studies were reviews and meta-analyses focusing on terrestrial ecosystems and providing general guidelines to manage invasive species at the national (6.5% out of the 388 documents), supranational/global (5.3%) and regional scales (4.3%) (Figure 5). They were followed by field experiments (manipulative) on terrestrial ecosystems addressed to locally eradicate specific taxa (3.3%). Reviews and meta-analyses on inland waters and those providing general guidelines to manage IAS at higher scales (i.e. regional to supranational/global) were also frequent (3.2% and 2.8%, respectively). Field experiments (manipulative) in inland waters addressed to eradicate (3.0%) or control (2.8%) specific taxa were in all cases local. The most frequent observational field studies on both terrestrial ecosystems (2.3%) and inland waters (2.0%) addressed generic aspects and were local. In contrast, documents focusing on marine ecosystems were scarce and studied generic aspects of marine invasion science with supranational/global (1.0%) or local (0.9%) perspectives. Manipulative field experiments to locally eradicate marine species were markedly rare (0.3%). Studies in urban environments were mostly reviews and meta-analyses addressing generic aspects at both supranational/global and local scales were the most abundant (0.5% and 0.5%, respectively). The proportion of field manipulative experiments to eradicate or control species was negligible. 134 Rafael Mufioz-Mas et al. / NeoBiota 70: 123—150 (2021) Supranational/global h ‘ \ : T- IOs National Field exp.{(manipulative) a, m@Greenhouse/lab\exp. _— WSS f & _ | ; Local Obs: field study 0 eo (Urban “_ ~—=sa eel Other Figure 5. Alluvial diagram relating the methodological approach, ecosystem type, management topic and spatial scale of the compiled documents on invasive alien species (IAS) management in Spain. Con- nection width is proportional to the number of documents (An interactive version of this figure can be downloaded from https://doi.org/10.6084/m9.figshare. 16547790.v1). The most frequent approaches, described within terrestrial studies, focused on aware- ness-raising, survey/monitoring and regulation (7.3%, 6.8% and 3.1%, respectively out of the 388 documents). Most of them had no quantifiable (not applicable/17.2%) or un- known success (2.1%). ‘This was followed by the use of biocontrol agents whose efficacy has not yet been tested (i.e. unknown, 1.6%) and unsuccessful culling of IAS (none and partial, 1.7%). The successful approaches most frequently reported combined herbicides and mechanical and manual plant removal (2.9% in total). In inland waters, awareness- raising and regulation were amongst the most frequently indicated approaches (3.9% and 3.0%, respectively), although with no quantifiable success (not applicable, 6.9%). Water level and flow regime manipulation was the most frequent management approach, but it was not tested (unknown, 2.3%) and occasionally turned out useless (0.7%). Cull- ing and poisoning seldom worked (0.8% and 0.5%, respectively) and the success of most reported experiences was unknown or partial (1.6% and 0.9%, respectively). Hydrogeo- morphological restoration, re-afforestation, plant removal and herbicide use were the most common approaches to control invasive riparian vegetation (1.2%, 1.1%, 1.6% and 0.7%, respectively). However, success of these treatments was partial or uncertain and only 0.6% reported successful experiences. The treatments for marine ecosystems fol- lowed a similar pattern and focused on preventative approaches: awareness-raising, sur- vey/monitoring and regulation (1.9%, 1.0% and 0.9%, respectively), most of them with no quantifiable (not applicable/2.0%) or unknown success (1.6%). The only successful study involved raising awareness and DNA metabarcoding to confirm the elimination of the pygmy mussel (Xenostrobus securis) (Miralles et al. 2016). Awareness-raising, regula- tion and survey/monitoring were the most common approaches for urban environments (3.7% in total), but the few applied experiences indicated partial success through culling and plant removal and subsequent herbicide spraying (0.3%). Review of invasive alien species management literature from Spain 135 ——, se Awareness raising eee Not applicable Unknown ifforestation Exclosure. ses a, Se . : 7 = —<—= QoS — ‘@) — — les i s ee = Othe == SS Mechanical,removal—= Partial Hydrology manipulation _ “=== ydrogeomorphological restoratio mS P g — ratlol’ | Yes Figure 6. Alluvial diagram relating the ecosystem type, treatment and success of the compiled documents on invasive alien species (IAS) management in Spain. Connection width is proportional to the number of documents. The category Other includes mulching, prevention, sterilisation, heating, incineration, con- tainment, baiting, restocking, DNA metabarcoding, insecticide and genetic selection (Alternative static and interactive versions of this figure relating species/taxa, treatment and success can be downloaded from https://doi.org/10.6084/m9. figshare. 16547790.v1). The collected keywords encompassed 1,145 different terms. The aggregation al- gorithm revealed 39 different research areas or clusters (Figure 7A), with 67 keywords occurring on 2 4 occasions (Figure 7B). The largest research area highlighted the im- portance of invasive plants amongst the Spanish literature on IAS management, the Mediterranean nature of much of the territory and the numerous studies carried out on this taxon in the Balearic Islands. The simplified network reflected the main top- ics of the study: invasive species and management, eradication and control. It also reflected research carried out on specific taxa, such as on the elimination of American mink (Neovison vison), which clustered with invasive species. Exclusion experiments on the European rabbit (Oryctolagus cuniculus) and feral cats (Felis silvestris catus) appeared in different research areas. The studies on feral cats were undertaken mainly in the Ca- nary Islands as their research areas were connected. In addition, the resulting network highlighted the impacts on freshwater biodiversity caused by giant reed (A. donax) and aquaculture activities. The simplified network reflected the importance of the yellow- legged hornet (V. velutina) and mosquitoes (mainly the tiger mosquito A. albopictus) and the extensive use of species distribution models (SDMs), such as MaxEnt (Phillips et al. 2004), to foresee expansion trends and suitable regions. Specific topics (propagule pressure and ecosystem services) and introduction vectors (ballast waters, aquaculture and hunting) appeared in separate research areas. The simplified network reflected specific management approaches, such as general forest management, use of herbicides or emergence of citizen science. It also reflected studies addressing the interaction be- 136 Rafael Mufioz-Mas et al. / NeoBiota 70: 123—150 (2021) ms wetland e yt ee ballast citizen 2 -eucalyt tus Bs lobulus : aed\ _ Scienc. Shredder fos Lesved oe ones fra ment /. ‘Idlif s ba non-nat / MWIHIAdIl =r . at _gibratar —/ salt oe ; _-marsh i —" ; feat i ‘SU rveil/ LL TS" 7 environment interview >< Q,. or number of occurrences 2 4). Overall vertex sizes are proportional to the log-transformed number of occurrences and inner circles to the proportion within each research area. Label sizes have been rescaled to avoid overlapping. tween invasions and climate change. In addition to the main toponymy used during the bibliography search, the network reflected specific regions and environments, such as the Strait of Gibraltar and Galicia (NW Spain) and the importance of wetlands and salt marshes. Moreover, the simplified network highlighted the importance of the ar- chipelagos and islands within Spanish invasion science research, given that island and Canary Islands appear in differentiated research areas. It also revealed the multiplicity of terms used to name similar concepts, such as the terms alien species and exotic spe- cies that appear scattered throughout different research areas. Discussion Spanish literature on IAS management has been mainly theoretical (55% review/meta- analysis), with a balance between theoretical and applied studies similar to that report- ed in other studies on biological and ecological aspects of biological invasions (Andreu and Vila 2007; Bayliss et al. 2013; Matzek et al. 2014, 2015). Nonetheless, IAS man- Review of invasive alien species management literature from Spain 137 agement literature has been under-represented compared to the Spanish and global trends on scientific production, although recently its share has grown. Altogether, this suggests that Spanish invasion science may also suffer from a knowing-doing gap caused by a preponderance of theoretical studies (Matzek et al. 2014, 2015). Moreo- ver, scientific papers written in English constituted a large proportion of the compiled literature, which suggests that most of it may be too scientifically orientated to be directly applied (Andreu and Vila 2007; Mungi et al. 2019; Copp et al. 2021). Never- theless, scientific activity in Spain has also incorporated new forecasting technologies (e.g. SDMs/MaxEnt, de Medeiros et al. 2018) along with new approaches to engage society in IAS control (e.g. citizen science, Clusa et al. 2018) and for biomonitoring (e.g. DNA metabarcoding, Borrell et al. 2017). In addition, risk assessments and hori- zon scanning studies for decision-making formed a notable part of the literature, with direct implications for IAS regulation (Bayon and Vila 2019). There was also discus- sion regarding the inefficiency of current codes of conduct and laws (Maceda-Veiga et al. 2013), aimed at enforcing policies to overcome the highlighted deficiencies. The proportion of applied studies and field experiments was markedly low, which impeded rating the efficacy of most of the described approaches (66.2%). Moreover, studies on novel biocontrol agents, such as the use of pathogens (McColl and Sunarto 2020) were infrequent. In part, this is because these agents require rigorous risk assess- ment studies and are, hence, subject to strict regulations (Loomans 2021). Thus, species eradication and control experiences often relied on the use of herbicides, mechanical elimination or culling (e.g. Melero et al. 2010; Mateos-Naranjo et al. 2012) and success- ful approaches were restricted to small-scale areas, such as islets and ponds (e.g. Ferreras- Romero et al. 2016; Maceda-Veiga et al. 2017). Consequently, concerns of Spanish man- agers about the problem that too much research focuses generally on the ecological as- pects of alien plants, rather than on specific cost-eficient management strategies (Andreu et al. 2009), can be considered, to some extent, applicable to most invasive alien taxa. The proportion of documents per species and ecosystem type in Spain was similar to that estimated in other countries (Thomsen et al. 2014). Terrestrial species, mainly plants, attracted the bulk of the literature, followed by studies involving species of inland waters. By contrast, marine and urban environments were infrequent in the collected literature. The preponderance of terrestrial ecosystems and the associated spe- cies can be justified by the primary introduction pathways of terrestrial species (i.e. release and/or escape), which are largely related to forestry, livestock, agriculture and wildlife trade (Essl et al. 2015). Vascular plants are the most frequently introduced taxon worldwide; consequently, they were expected to receive the largest proportion of studies. However, the feasibility of managing terrestrial invaders or aliens, espe- cially sessile species and stages of their life history (e.g. nests, Enriquez et al. 2013), is greater compared to aquatic species, due to the lower accessibility of these environ- ments. Therefore, a publication bias towards successful studies with positive results on tractable terrestrial species is not discernible (Fanelli 2012; Booy et al. 2017). Studies on terrestrial ecosystems involved all spatial scales (i.e. local, regional, na- tional and supranational). However, applied experiments and experience were mostly 138 Rafael Mufioz-Mas et al. / NeoBiota 70: 123—150 (2021) local interventions, such as management of prickly pear species (Opuntia spp.) and the sentry plant (Agave americana) (Arévalo et al. 2015). By contrast, eradication and control of vagile terrestrial organisms proved to be economically unaffordable (e.g. American mink NV. vison, Melero et al. 2010; Manas et al. 2016), especially in a con- text of multilevel overlapping or competing public administrations with ill-defined jurisdictions and pervasive budget shortages (Tollington et al. 2017; Dana et al. 2019). In this regard, island territories were well covered by the collected literature, with sev- eral successful management experiences in these territories, such as the eradication of American mink (JV. vison) in the Atlantic Islands National Park (Velando et al. 2017) or of the red palm weevil (R. ferrugineus) from the Canary Islands (Fajardo et al. 2019). Impacts of IAS on islands are likely to increase in the future, especially on oceanic islands, such as the Canaries and, to a lesser extent, on the continental Balearic Archipelago. Indeed, insular terrestrial ecosystems are generally the most threatened (Lenzner et al. 2020). Therefore, these two successful examples shed hope on the future management of IAS in Spanish insular territories. The published research on terrestrial invertebrates and microorganisms appeared to be concentrated on a few species with direct impacts on economics and human health (e.g. yellow-legged hornet V. velutina, pinewood nematode B. xylophilus or tiger mosquito A. albopictus). However, further applied research and knowledge transfer is particularly needed to control invertebrates, due to the rising number of introduc- tions worldwide (Saul et al. 2017; Seebens 2019). Such a task often requires strategies based on prevention and prompt eradication (e.g. ballast water sanitation) (Booy et al. 2017, 2020), but these were the least frequent of the categories amongst those imply- ing direct manipulation of the target taxa. From a theoretical viewpoint, the compiled literature raises awareness and proposes changes to current regulations as its main approach, directed at preventing further introductions at a higher level of organisa- tion. Legislation regarding IAS has become more restrictive over the years worldwide and Spain is also immersed in this useful trend (Turbelin et al. 2017; Maceda-Veiga et al. 2019). However, in light of the number of recent introductions (Mufoz-Mas and Garcfa-Berthou 2020), it can be concluded that the real effective capability of Spain to impede the establishment of further species is limited. This general pattern is shared with other European countries and is unlikely to change substantially in the near future (Seebens et al. 2021). Tackling the establishment of further terrestrial invertebrates and microorganisms will require further and stronger innovative and well-funded preventative approaches. The number of studies conducted in inland waters was notably high due to the enormous number of established species and their associated economic costs (e.g. Duran et al. 2012; Mufioz-Mas and Garcia-Berthou 2020). Some of this research was promoted by the Water Framework Directive (European Parliament & Council 2000), even if IAS are not explicitly mentioned therein (Boon et al. 2020). Our keyword co- occurrence network reflected the numerous studies recommending flow management as a way to control IAS (Sabater et al. 2008; Fornaroli et al. 2020). However, despite the schemes conducted in other countries (Kiernan et al. 2012), no applied examples Review of invasive alien species management literature from Spain 139 in large and intermediate regulated river systems were found in the literature. River basin management plans increasingly account for the presence of IAS, but more em- phasis on applied management of medium-to-large river systems is necessary (Boon et al. 2020). Nonetheless, applied studies of inland water ecosystems dealt with control of the giant reed A. donax (the most managed species appearing in the compiled litera- ture) in relatively small areas (Bruno et al. 2019) or described experience in relatively small lentic environments (i.e. common carp Cyprinus carpio in ponds and lakes; Fer- reras-Romero et al. 2016) and small streams (signal crayfish Pacifastacus leniusculus; Dana et al. 2010). Unfortunately, more research is needed to optimise water alloca- tion schemes because climate change is facilitating the establishment of further IAS. Meanwhile, the increased demands of agriculture will reduce the availability of water resources to undertake the aforementioned actions (Rahel and Olden 2008; Escribano Francés et al. 2017). In Spain, stowaway introductions in brackish and marine environments have also gained prominence (Garcia-Gomez et al. 2020; Painting et al. 2020), caus- ing a shift in the type of introduced species that can be framed within the cur- rent increase in global maritime traffic (Saul et al. 2017; Seebens 2019). In this regard, Spain enacted in 2004 the International Convention for the Control and Management of Ships’ Ballast Water and Sediments (BWM Convention), which has been addressed in local studies (e.g. Moreno-Andrés et al. 2017), dissertations (e.g. Bartolomé Lamarca 2014) and is highlighted in the keyword co-occurrence network. However, new IAS records are being reported frequently. For example, the gastropod Mitrella psilla was recently found thriving on western coasts of Spain (Martinez-Orti et al. 2020). The effectiveness of measures to fulfil the BWM Con- vention remains limited, which underscores the difficulties faced in managing ma- rine LAS (Thomsen et al. 2014; Cuesta et al. 2016). Indeed, the number of first re- cords whose most probable introduction pathways are ballast waters or biofouling (Davidson et al. 2018) and the increasing importance of aquaculture and related introductions (Nunes et al. 2015; Garlock et al. 2020) suggest these introduction pathways must be taken into account. It can, therefore, be concluded that marine invasion science should move towards our central focus in the future. Worldwide, urban environments are becoming active introduction hubs (Gaert- ner et al. 2017). Indeed, there are several examples of initial IAS establishment in urban zones that have spread outwards over natural environments in Spain, such as Lippia filiformis (Casasayas i Fornell 1989) or the black-headed weaver Ploceus mel- anocephalus (Grundy et al. 2014). Ornamental plants and alien exotic birds kept as pets are perhaps the most striking and troublesome introductions in city surround- ings (Riera et al. 2021), but other less-known taxa have been found on numerous occasions (e.g. Pseudosuccinea columella (Mollusca) Martinez-Orti 2013). Besides the introduction of ornamental plants and tortoises and terrapins (Trachemis spp.), which have already spread over natural environments and prompted specific studies (Mufioz- Mas and Garcia-Berthou 2020), the majority of Spanish management literature on urban environments has focused on birds (e.g. the monk parakeet Myiopsitta monachus 140 Rafael Mufioz-Mas et al. / NeoBiota 70: 123—150 (2021) and the rose-ringed parakeet Psittacula krameri (Alvarez-Pola and Muntaner 2009; Maceda-Veiga et al. 2019; Hernandez-Brito et al. 2020; Saavedra and Medina 2020). Therefore, in the light of increasing urbanisation of the Spanish population and the relatively low number of specific studies, we conclude that prevention protocols and further studies, specifically addressed to urban environments, should be strengthened to encompass the full spectrum of potential introductions. The compiled literature on IAS management in Spain does not particularly reflect budget reductions related to the Great Recession of 2008 (Catanzaro 2018). However, IAS management literature has been under-represented compared to overall scientific production trends and the current rise in publication rates has not compensated for this historical delay. Nonetheless, our compiled references only represent a small frac- tion of the total number of reviewed documents (388/3796 = 10.22%). Moreover, a significant number of documents were written in Spanish (n = 158; 40.7%). This finding deserves special attention as it handicaps knowledge transfer (Di Bitetti and Ferreras 2017) and biases conclusions inferred by international agents (Konno et al. 2020). However, it is not problematic from a national point of view because texts, documents and software packages assisting the process of decision-making by adminis- trators and functionaries have proven to be most efhcient when presented in local lan- guages (Copp et al. 2021). Nevertheless, despite the proliferation of public repositories and open access publications, a wealth of information is still hidden away, not easily accessible to risk assessors, managers and researchers through standard search engines. For example, it is known that more than a hundred plant species have been managed by Spanish regional administrations (Andreu and Vila 2007), but only the most fre- quent species generated accessible documents (e.g. reports). Altogether, it indicates that public agencies produce insufficient literature (sensu lato) as they focus on other tasks. Neither communication between managers and scientists beyond undertaking management action schemes nor protocols to evaluate their success are common prac- tices in Spain. It would be beneficial for public agencies to encourage and facilitate such interguild contact, perhaps using legislative and labour changes, to disseminate applied experience in accessible ways. Despite these recommendations and the highlighted deficiencies, Spanish literature on IAS management should not be considered completely defective. Recent studies on alien animal species, currently thriving in Spanish inland waters, indicate that no single management protocol can be applied to every taxonomic group, due to marked differ- ences amongst species, introduction pathways and invaded habitats (Mufioz-Mas and Garcia-Berthou 2020). Likewise, our study shows a strong association between species, taxon or group of taxa and the features/categories used to describe the compiled litera- ture. This indicates that species-specific studies are often needed, which highlights how difficult and complex the task of IAS management is (Woodford et al. 2016; Portela et al. 2020; Yelenik et al. 2020). Our results should help to properly drive future research efforts towards IAS management in Spain. We recommend more research into applied techniques to shift the balance between theoretical and empirical studies, especially in inland waters and marine ecosystems due to their lower accessibility. The same need for Review of invasive alien species management literature from Spain 141 more studies applies to urban environments, as they are often the bridgehead of LAS introductions. Renewed effort in prevention and prompt eradication should be made to fulfil, for example, the BWM Convention and impede further introductions into marine ecosystems. 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In: Plant invasions: the role of biotic interactions. CABI, 402-420. https://doi. org/10.1079/9781789242171.0402 150 Rafael Mufioz-Mas et al. / NeoBiota 70: 123—150 (2021) Zenni RD, Essl K, Garcia-Berthou E, McDermott SM (2021) The economic costs of bio- logical invasions around the world. NeoBiota 67: 1-9. https://doi.org/10.3897/neobio- ta.67.69971 Zhao H, Lu L (2015) Variational circular treemaps for interactive visualization of hierarchical data. In: Liu $, Scheuermann G, Takahashi S (Eds) 2015 IEEE Pacific Visualization Sym- posium (PacificVis). Institute of Electrical and Electronics Engineers (IEEE), Hangzhou (China), 81-85. https://doi.org/10.1109/PACIFICVIS.2015.7156360 Supplementary material | Complete reference list and the features used to characterise the references Authors: Rafael Mufioz-Mas, Martina Carrete, Pilar Castro-Diez, Miguel Delibes- Mateos, Josep A. Jaques, Marta Lopez-Darias, Manuel Nogales, Joan Pino, Anna Traveset, Xavier Turon, Montserrat Vila, Emili Garcia-Berthou. Data type: references and features Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODDbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/neobiota.70.68202.suppl1 Supplementary material 2 Table S1. Table of features, categories and definitions used to characterise the compiled literature Authors: Rafael Mufioz-Mas, Martina Carrete, Pilar Castro-Diez, Miguel Delibes- Mateos, Josep A. Jaques, Marta Lopez-Darias, Manuel Nogales, Joan Pino, Anna Traveset, Xavier Turon, Montserrat Vila, Emili Garcia-Berthou Data type: definitions Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODDbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.3897/neobiota.70.68202.suppl2